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Characteristics of the Urinary Microbiome in Kidney Stone Patients

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Characteristics of the Urinary Microbiome in Kidney Stone Patients Liu et al. J Transl Med (2020) 18:130 https://doi.org/10.1186/s12967-020-02282-3 Journal of Translational Medicine RESEARCH Open Access Characteristics of the urinary microbiome in kidney stone patients with hypertension Fengping Liu1,2†, Nan Zhang2†, Peng Jiang2†, Qixiao Zhai3†, Chen Li2, Deshui Yu2, Yan Wu2, Yuwei Zhang2, Longxian Lv4*, Xinyu Xu2* and Ninghan Feng2* Abstract Background: Kidney stone disease (KSD) is more common in individuals with hypertension (HTN) than in individuals with normotension (NTN). Urinary dysbiosis is associated with urinary tract disease and systemic diseases. However, the role of the urinary microbiome in KSD complicated with HTN remains unclear. Methods: This study investigated the relationship between the pelvis urinary microbiome and blood pressure (BP) in patients with KSD co-occurring with HTN (KSD-HTN) and healthy controls (HC) by conducting 16S rRNA gene sequencing of bacteria in urine samples. The urine samples were collected (after bladder disinfection) from 50 patients with unilateral kidney calcium stones and NTN (n 12), prehypertension (pHTN; n 11), or HTN (n 27), along with 12 HCs. = = = Results: Principal coordinates analysis showed that there were signifcant diferences in the urinary microbiomes not only between KSD patients and HCs but also between KSD-pHTN or KSD-HTN patients and KSD-NTN patients. Gardnerella dominated in HCs, Staphylococcus dominated in KSD-NTN patients and Sphingomonas dominated in both KSD-pHTN and KSD-HTN patients. The abundance of several genera including Acidovorax, Gardnerella and Lactobacil- lus was correlated with BP. Adherens junction and nitrogen and nucleotide metabolism pathways, among others, were associated with changes in BP. Conclusions: The fndings suggest that patients with KSD complicated with HTN have a unique urinary microbiome profle and that changes in the microbiome may refect disease progression and may be useful to monitor response to treatments. Keywords: Kidney pelvis, Kidney stone disease, Microbiome, Hypertension, Prehypertension, Urinary bacteria Background Kidney stone disease (KSD) is common, with a preva- lence of up to 14.8%, which is increasing over time, and a recurrence rate of up to 50% within the frst 5 years of *Correspondence: [email protected]; [email protected]; the initial episode [1]. KSD disproportionately afects [email protected] †Fengping Liu, Nan Zhang, Peng Jiang and Qixiao Zhai contributed patients with hypertension (HTN) compared to individu- equally to this work als with normal blood pressure (BP), i.e. normotension 2 Department of Urology, Afliated Wuxi No. 2 Hospital, Nanjing Medical (NTN) [2]. Both KSD and HTN impair kidney function; University, Wuxi, Jiangsu, China 4 State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, this can lead to chronic kidney disease, which negatively National Clinical Research Center for Infectious Diseases, Collaborative afects quality of life and can be fatal [3, 4]. Innovation Center for Diagnosis and Treatment of Infectious Diseases, Clarifying the shared pathophysiologic basis of KSD The First Afliated Hospital, College of Medicine, Zhejiang University, Hangzhou, Zhejiang, China and HTN could lead to more efective treatments for Full list of author information is available at the end of the article patients. In KSD patients, HTN was previously found to © The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Liu et al. J Transl Med (2020) 18:130 Page 2 of 13 be associated with signifcantly increased urine calcium this hypothesis by comparing the urinary microbiome [5], which may result in low blood calcium. Adequate cal- profles (based on bacterial 16S rRNA gene sequenc- cium levels may regulate BP by modifying intracellular ing of urine samples) of healthy controls (HCs) and KSD calcium in vascular smooth muscle cells and by varying patients with NTN, prehypertension (pHTN) and HTN. the blood volume via the renin–angiotensin–aldoster- Te results demonstrate that the co-occurrence of HTN one system. Low blood calcium can increase the activ- alters the urinary microbiome composition of KSD ity of the parathyroid gland, and parathyroid hormone patients, which has important implications for disease increases intracellular calcium in vascular smooth mus- diagnosis and management. cles, resulting in vasoconstriction. Low blood calcium also increases the synthesis of calcitriol in a direct man- Methods ner or via parathyroid hormone, and calcitriol increases Subject recruitment intracellular calcium in vascular smooth muscle cells. Kidney stone disease patients who were undergoing ure- Low blood calcium may stimulate renin release and teroscopic lithotripsy were recruited and classifed into consequently increase the levels of angiotensin II and the following three groups according to BP: KSD-NTN, aldosterone [6], which are responsible for regulating BP. KSD-pHTN and KSD-HTN. Te presence of kidney Recent studies revealed that angiotensin II-induced HTN stones was confrmed by abdominal X-ray, ultrasonog- is associated with gut microbial composition and metab- raphy and computed tomography (CT), and calcium olites [7, 8]. stones were identifed by CT scans. Normal BP was Research has shown that human urine harbors its own defned as a systolic blood pressure (SBP) ≤ 120 mmHg microbial community, which has challenged the long- or a diastolic blood pressure (DBP) ≤ 80 mmHg; pHTN held notion that urine is sterile in the absence of infection was defned as an SBP of 120–139 mmHg or a DBP of [9]. Just as the gut, oral cavity and vaginal microbiomes 80–89 mmHg without the use of antihypertensive medi- contribute to human health, the urinary microbiome is cation; and HTN was defned as an SBP ≥ 140 mmHg or critical for the maintenance of physiologic homeostasis, a DBP ≥ 90 mmHg and/or use of antihypertensive medi- as demonstrated by the urinary dysbiosis observed in cation [20]. In addition, a cohort of subjects with neither prostate cancer [10], bacterial vaginosis [11] and neuro- stones nor HTN was recruited as the HC group. Exclu- pathic bladder [12]. sion criteria for patients and HCs were as follows: men- Te urinary metabolite profle of KSD patients with struation, pregnancy, cancer, heart failure, renal failure, HTN difers from that of KSD patients with NTN. For peripheral artery disease, urinary tract disease, urinary example, it was reported that uric acid, oxalic acid, titrat- tract deformity, known urinary tract infection (UTI) able acid and ammonium were increased in the urine based on clinical assessment, urinary catheterization of patients with calcium stones plus HTN compared to within the previous 4 weeks and treatment with antibiot- calcium stones plus NTN, whereas urinary pH and cit- ics within the previous 4 weeks. rate were decreased [13–15]. Tese changes can afect the urinary environment and, consequently, the relative Urine sample collection and DNA extraction abundance of bacteria in the urinary microbiome. Along Urine sample collection procedures for the KSD patients with being present in bladder urine, microorganisms were as follows: bladder urine was aspirated using a cys- populate urine in the upper urinary tract. toscope (Richard Wolf, Knittlingen, Germany) and the Recent studies have indicated the plausible involve- bladder was then disinfected three times with iodophor; ment of human microbiomes (in various body sites) in 2 mL of the last iodophor fush was used for expanded the regulation of BP. For example, in HTN patients, both quantitative urine culture (EQUC) [21] and patients with Yang et al. and Li et al. found that BP was associated with a positive EQUC (> 10 colony-forming units/mL of urine) dramatically decreased gut microbial richness and diver- were excluded [21]. After the last iodophor fush, nor- sity and bacterial composition [16, 17]. In another study mal saline was injected into the bladder and immediately on the oral microbiome, Ko et al. [18] demonstrated that aspirated to remove any iodophor solution remaining in obstructive sleep apnea/hypopnea syndrome (OSAHS) the bladder. Tis step was repeated three times and 3 mL patients with HTN had a diferent bacterial profle from urine was then aspirated from the kidney pelvis using a those without HTN. ureteroscope. As the procedure for the collection of kid- Given the interactions between the human microbiome ney pelvis urine samples was too invasive to obtain con- and the metabolome [19] and between the gut and oral sent from HCs and ethics approval from the hospital
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